Allosteric Modulation of NMDARs Reverses Patients' Autoantibody Effects in Mice.


Journal

Neurology(R) neuroimmunology & neuroinflammation
ISSN: 2332-7812
Titre abrégé: Neurol Neuroimmunol Neuroinflamm
Pays: United States
ID NLM: 101636388

Informations de publication

Date de publication:
01 2022
Historique:
received: 03 09 2021
accepted: 21 10 2021
entrez: 14 12 2021
pubmed: 15 12 2021
medline: 12 3 2022
Statut: epublish

Résumé

To demonstrate that an analog (SGE-301) of a brain-derived cholesterol metabolite, 24(S)-hydroxycholesterol, which is a selective positive allosteric modulator (PAM) of NMDA receptors (NMDARs), is able to reverse the memory and synaptic alterations caused by CSF from patients with anti-NMDAR encephalitis in an animal model of passive transfer of antibodies. Four groups of mice received (days 1-14) patients' or controls' CSF via osmotic pumps connected to the cerebroventricular system and from day 11 were treated with daily subcutaneous injections of SGE-301 or vehicle (no drug). Visuospatial memory, locomotor activity (LA), synaptic NMDAR cluster density, hippocampal long-term potentiation (LTP), and paired-pulse facilitation (PPF) were assessed on days 10, 13, 18, and 26 using reported techniques. On day 10, mice infused with patients' CSF, but not controls' CSF, presented a significant visuospatial memory deficit, reduction of NMDAR clusters, and impairment of LTP, whereas LA and PPF were unaffected. These alterations persisted until day 18, the time of maximal deficits in this model. In contrast, mice that received patients' CSF but from day 11 were treated with SGE-301 showed memory recovery (day 13), and on day 18, all paradigms (memory, NMDAR clusters, and LTP) had reversed to values similar to those of controls. On day 26, no differences were observed among experimental groups. An oxysterol biology-based PAM of NMDARs is able to reverse the synaptic and memory deficits caused by CSF from patients with anti-NMDAR encephalitis. These findings suggest a novel adjuvant treatment approach that deserves future clinical evaluation.

Sections du résumé

BACKGROUND AND OBJECTIVES
To demonstrate that an analog (SGE-301) of a brain-derived cholesterol metabolite, 24(S)-hydroxycholesterol, which is a selective positive allosteric modulator (PAM) of NMDA receptors (NMDARs), is able to reverse the memory and synaptic alterations caused by CSF from patients with anti-NMDAR encephalitis in an animal model of passive transfer of antibodies.
METHODS
Four groups of mice received (days 1-14) patients' or controls' CSF via osmotic pumps connected to the cerebroventricular system and from day 11 were treated with daily subcutaneous injections of SGE-301 or vehicle (no drug). Visuospatial memory, locomotor activity (LA), synaptic NMDAR cluster density, hippocampal long-term potentiation (LTP), and paired-pulse facilitation (PPF) were assessed on days 10, 13, 18, and 26 using reported techniques.
RESULTS
On day 10, mice infused with patients' CSF, but not controls' CSF, presented a significant visuospatial memory deficit, reduction of NMDAR clusters, and impairment of LTP, whereas LA and PPF were unaffected. These alterations persisted until day 18, the time of maximal deficits in this model. In contrast, mice that received patients' CSF but from day 11 were treated with SGE-301 showed memory recovery (day 13), and on day 18, all paradigms (memory, NMDAR clusters, and LTP) had reversed to values similar to those of controls. On day 26, no differences were observed among experimental groups.
DISCUSSION
An oxysterol biology-based PAM of NMDARs is able to reverse the synaptic and memory deficits caused by CSF from patients with anti-NMDAR encephalitis. These findings suggest a novel adjuvant treatment approach that deserves future clinical evaluation.

Identifiants

pubmed: 34903638
pii: 9/1/e1122
doi: 10.1212/NXI.0000000000001122
pmc: PMC8669659
pii:
doi:

Substances chimiques

Autoantibodies 0
Hydroxycholesterols 0
24-hydroxycholesterol 47IMW63S3F

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

Copyright © 2021 The Author(s). Published by Wolters Kluwer Health, Inc. on behalf of the American Academy of Neurology.

Références

Neurol Neuroimmunol Neuroinflamm. 2019 Oct 16;7(1):
pubmed: 31619447
Brain. 2020 Sep 1;143(9):2709-2720
pubmed: 32830245
Epilepsy Behav. 2020 Jul;108:107088
pubmed: 32375094
Eur J Paediatr Neurol. 2019 Jan;23(1):7-18
pubmed: 30318435
Eur J Paediatr Neurol. 2020 Nov;29:87-91
pubmed: 33046392
Eur J Neurol. 2016 Mar;23(3):621-9
pubmed: 26563553
Lancet Neurol. 2011 Jan;10(1):63-74
pubmed: 21163445
Epilepsy Behav. 2020 Jul;108:107066
pubmed: 32375097
J Neurosci. 2018 Mar 28;38(13):3218-3229
pubmed: 29476014
Expert Rev Clin Immunol. 2010 Nov;6(6):867-74
pubmed: 20979551
Ann Neurol. 2021 Nov;90(5):725-737
pubmed: 34562035
Lancet Neurol. 2008 Dec;7(12):1091-8
pubmed: 18851928
Ann Neurol. 2016 Sep;80(3):388-400
pubmed: 27399303
Lancet Neurol. 2013 Feb;12(2):157-65
pubmed: 23290630
Am J Respir Crit Care Med. 2017 Feb 15;195(4):491-499
pubmed: 27552490
Neurocrit Care. 2018 Oct;29(2):264-272
pubmed: 29651625
J Neurosci. 2013 Oct 30;33(44):17290-300
pubmed: 24174662
Brain. 2015 Jan;138(Pt 1):94-109
pubmed: 25392198
Ann Neurol. 2009 Jul;66(1):11-8
pubmed: 19670433
J Neurol Neurosurg Psychiatry. 2012 Feb;83(2):195-8
pubmed: 21933952
Brain. 2010 Jun;133(Pt 6):1655-67
pubmed: 20511282
Neurology. 2018 May 29;90(22):e1997-e2005
pubmed: 29703768
Br J Pharmacol. 2007 Jan;150(2):164-75
pubmed: 17160009
Ann Neurol. 2014 Jul;76(1):108-19
pubmed: 24916964
J Neurosci. 2010 Apr 28;30(17):5866-75
pubmed: 20427647
Neurology. 2014 Feb 18;82(7):556-63
pubmed: 24443452
Neurology. 2020 Aug 11;95(6):e671-e684
pubmed: 32576635
Lancet Neurol. 2019 Nov;18(11):1045-1057
pubmed: 31326280
Semin Neurol. 2003 Jun;23(2):191-8
pubmed: 12894384
Lancet Neurol. 2014 Feb;13(2):167-77
pubmed: 24360484

Auteurs

Marija Radosevic (M)

From the Institut d'Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS) (M.R., J.P., F.M., A.M., E.A., L.S., J.L., A.G.-S., E.M., X.G., J.D.), Hospital Clínic, Universitat de Barcelona, Barcelona, Spain; Laboratori de Neurofisiologia (X.G.), Departament de Biomedicina, Facultat de Medicina i Ciències de la Salut, Institut de Neurociències, Universitat de Barcelona, Barcelona, Spain; Sage Therapeutics (M.L.), Department of Research and Nonclinical Development, Cambridge, MA; Department of Neurology (J.D.), University of Pennsylvania, Philadelphia, PA; Centro de Investigación Biomédica en Red de Enfermedades Raras (CIBERER) (J.D.), Madrid, Spain; and Institució Catalana de Recerca i Estudis Avançats (ICREA) (J.D.), Barcelona, Spain.

Jesús Planagumà (J)

From the Institut d'Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS) (M.R., J.P., F.M., A.M., E.A., L.S., J.L., A.G.-S., E.M., X.G., J.D.), Hospital Clínic, Universitat de Barcelona, Barcelona, Spain; Laboratori de Neurofisiologia (X.G.), Departament de Biomedicina, Facultat de Medicina i Ciències de la Salut, Institut de Neurociències, Universitat de Barcelona, Barcelona, Spain; Sage Therapeutics (M.L.), Department of Research and Nonclinical Development, Cambridge, MA; Department of Neurology (J.D.), University of Pennsylvania, Philadelphia, PA; Centro de Investigación Biomédica en Red de Enfermedades Raras (CIBERER) (J.D.), Madrid, Spain; and Institució Catalana de Recerca i Estudis Avançats (ICREA) (J.D.), Barcelona, Spain.

Francesco Mannara (F)

From the Institut d'Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS) (M.R., J.P., F.M., A.M., E.A., L.S., J.L., A.G.-S., E.M., X.G., J.D.), Hospital Clínic, Universitat de Barcelona, Barcelona, Spain; Laboratori de Neurofisiologia (X.G.), Departament de Biomedicina, Facultat de Medicina i Ciències de la Salut, Institut de Neurociències, Universitat de Barcelona, Barcelona, Spain; Sage Therapeutics (M.L.), Department of Research and Nonclinical Development, Cambridge, MA; Department of Neurology (J.D.), University of Pennsylvania, Philadelphia, PA; Centro de Investigación Biomédica en Red de Enfermedades Raras (CIBERER) (J.D.), Madrid, Spain; and Institució Catalana de Recerca i Estudis Avançats (ICREA) (J.D.), Barcelona, Spain.

Araceli Mellado (A)

From the Institut d'Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS) (M.R., J.P., F.M., A.M., E.A., L.S., J.L., A.G.-S., E.M., X.G., J.D.), Hospital Clínic, Universitat de Barcelona, Barcelona, Spain; Laboratori de Neurofisiologia (X.G.), Departament de Biomedicina, Facultat de Medicina i Ciències de la Salut, Institut de Neurociències, Universitat de Barcelona, Barcelona, Spain; Sage Therapeutics (M.L.), Department of Research and Nonclinical Development, Cambridge, MA; Department of Neurology (J.D.), University of Pennsylvania, Philadelphia, PA; Centro de Investigación Biomédica en Red de Enfermedades Raras (CIBERER) (J.D.), Madrid, Spain; and Institució Catalana de Recerca i Estudis Avançats (ICREA) (J.D.), Barcelona, Spain.

Esther Aguilar (E)

From the Institut d'Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS) (M.R., J.P., F.M., A.M., E.A., L.S., J.L., A.G.-S., E.M., X.G., J.D.), Hospital Clínic, Universitat de Barcelona, Barcelona, Spain; Laboratori de Neurofisiologia (X.G.), Departament de Biomedicina, Facultat de Medicina i Ciències de la Salut, Institut de Neurociències, Universitat de Barcelona, Barcelona, Spain; Sage Therapeutics (M.L.), Department of Research and Nonclinical Development, Cambridge, MA; Department of Neurology (J.D.), University of Pennsylvania, Philadelphia, PA; Centro de Investigación Biomédica en Red de Enfermedades Raras (CIBERER) (J.D.), Madrid, Spain; and Institució Catalana de Recerca i Estudis Avançats (ICREA) (J.D.), Barcelona, Spain.

Lidia Sabater (L)

From the Institut d'Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS) (M.R., J.P., F.M., A.M., E.A., L.S., J.L., A.G.-S., E.M., X.G., J.D.), Hospital Clínic, Universitat de Barcelona, Barcelona, Spain; Laboratori de Neurofisiologia (X.G.), Departament de Biomedicina, Facultat de Medicina i Ciències de la Salut, Institut de Neurociències, Universitat de Barcelona, Barcelona, Spain; Sage Therapeutics (M.L.), Department of Research and Nonclinical Development, Cambridge, MA; Department of Neurology (J.D.), University of Pennsylvania, Philadelphia, PA; Centro de Investigación Biomédica en Red de Enfermedades Raras (CIBERER) (J.D.), Madrid, Spain; and Institució Catalana de Recerca i Estudis Avançats (ICREA) (J.D.), Barcelona, Spain.

Jon Landa (J)

From the Institut d'Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS) (M.R., J.P., F.M., A.M., E.A., L.S., J.L., A.G.-S., E.M., X.G., J.D.), Hospital Clínic, Universitat de Barcelona, Barcelona, Spain; Laboratori de Neurofisiologia (X.G.), Departament de Biomedicina, Facultat de Medicina i Ciències de la Salut, Institut de Neurociències, Universitat de Barcelona, Barcelona, Spain; Sage Therapeutics (M.L.), Department of Research and Nonclinical Development, Cambridge, MA; Department of Neurology (J.D.), University of Pennsylvania, Philadelphia, PA; Centro de Investigación Biomédica en Red de Enfermedades Raras (CIBERER) (J.D.), Madrid, Spain; and Institució Catalana de Recerca i Estudis Avançats (ICREA) (J.D.), Barcelona, Spain.

Anna García-Serra (A)

From the Institut d'Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS) (M.R., J.P., F.M., A.M., E.A., L.S., J.L., A.G.-S., E.M., X.G., J.D.), Hospital Clínic, Universitat de Barcelona, Barcelona, Spain; Laboratori de Neurofisiologia (X.G.), Departament de Biomedicina, Facultat de Medicina i Ciències de la Salut, Institut de Neurociències, Universitat de Barcelona, Barcelona, Spain; Sage Therapeutics (M.L.), Department of Research and Nonclinical Development, Cambridge, MA; Department of Neurology (J.D.), University of Pennsylvania, Philadelphia, PA; Centro de Investigación Biomédica en Red de Enfermedades Raras (CIBERER) (J.D.), Madrid, Spain; and Institució Catalana de Recerca i Estudis Avançats (ICREA) (J.D.), Barcelona, Spain.

Estibaliz Maudes (E)

From the Institut d'Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS) (M.R., J.P., F.M., A.M., E.A., L.S., J.L., A.G.-S., E.M., X.G., J.D.), Hospital Clínic, Universitat de Barcelona, Barcelona, Spain; Laboratori de Neurofisiologia (X.G.), Departament de Biomedicina, Facultat de Medicina i Ciències de la Salut, Institut de Neurociències, Universitat de Barcelona, Barcelona, Spain; Sage Therapeutics (M.L.), Department of Research and Nonclinical Development, Cambridge, MA; Department of Neurology (J.D.), University of Pennsylvania, Philadelphia, PA; Centro de Investigación Biomédica en Red de Enfermedades Raras (CIBERER) (J.D.), Madrid, Spain; and Institució Catalana de Recerca i Estudis Avançats (ICREA) (J.D.), Barcelona, Spain.

Xavier Gasull (X)

From the Institut d'Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS) (M.R., J.P., F.M., A.M., E.A., L.S., J.L., A.G.-S., E.M., X.G., J.D.), Hospital Clínic, Universitat de Barcelona, Barcelona, Spain; Laboratori de Neurofisiologia (X.G.), Departament de Biomedicina, Facultat de Medicina i Ciències de la Salut, Institut de Neurociències, Universitat de Barcelona, Barcelona, Spain; Sage Therapeutics (M.L.), Department of Research and Nonclinical Development, Cambridge, MA; Department of Neurology (J.D.), University of Pennsylvania, Philadelphia, PA; Centro de Investigación Biomédica en Red de Enfermedades Raras (CIBERER) (J.D.), Madrid, Spain; and Institució Catalana de Recerca i Estudis Avançats (ICREA) (J.D.), Barcelona, Spain.

Mike Lewis (M)

From the Institut d'Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS) (M.R., J.P., F.M., A.M., E.A., L.S., J.L., A.G.-S., E.M., X.G., J.D.), Hospital Clínic, Universitat de Barcelona, Barcelona, Spain; Laboratori de Neurofisiologia (X.G.), Departament de Biomedicina, Facultat de Medicina i Ciències de la Salut, Institut de Neurociències, Universitat de Barcelona, Barcelona, Spain; Sage Therapeutics (M.L.), Department of Research and Nonclinical Development, Cambridge, MA; Department of Neurology (J.D.), University of Pennsylvania, Philadelphia, PA; Centro de Investigación Biomédica en Red de Enfermedades Raras (CIBERER) (J.D.), Madrid, Spain; and Institució Catalana de Recerca i Estudis Avançats (ICREA) (J.D.), Barcelona, Spain.

Josep Dalmau (J)

From the Institut d'Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS) (M.R., J.P., F.M., A.M., E.A., L.S., J.L., A.G.-S., E.M., X.G., J.D.), Hospital Clínic, Universitat de Barcelona, Barcelona, Spain; Laboratori de Neurofisiologia (X.G.), Departament de Biomedicina, Facultat de Medicina i Ciències de la Salut, Institut de Neurociències, Universitat de Barcelona, Barcelona, Spain; Sage Therapeutics (M.L.), Department of Research and Nonclinical Development, Cambridge, MA; Department of Neurology (J.D.), University of Pennsylvania, Philadelphia, PA; Centro de Investigación Biomédica en Red de Enfermedades Raras (CIBERER) (J.D.), Madrid, Spain; and Institució Catalana de Recerca i Estudis Avançats (ICREA) (J.D.), Barcelona, Spain. jdalmau@clinic.cat.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH